SOIL ORGANIC MATTER TURNOVER IS GOVERNED BY ACCESSIBILITY NOT RECALCITRANCE - DESMOG
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Global Change Biology (2012) 18, 1781–1796, doi: 10.1111/j.1365-2486.2012.02665.x
INVITED REVIEW
Soil organic matter turnover is governed by accessibility
not recalcitrance
JENNIFER A. J. DUNGAIT*, DAVID W. HOPKINS*†2, ANDREW S. GREGORY‡
and A N D R E W P . W H I T M O R E ‡
*Department of Sustainable Soils and Grassland Systems, Rothamsted Research, North Wyke, Okehampton, Devon EX20 2SB,
UK, †School of Life Sciences, Heriot-Watt University, Edinburgh, EH14 4AS, UK, ‡Department of Sustainable Soils and
Grassland Systems, Rothamsted Research, Harpenden, Herts AL5 2LQ, UK
Abstract
Mechanisms to mitigate global climate change by sequestering carbon (C) in different ‘sinks’ have been proposed as
at least temporary measures. Of the major global C pools, terrestrial ecosystems hold the potential to capture and
store substantially increased volumes of C in soil organic matter (SOM) through changes in management that are also
of benefit to the multitude of ecosystem services that soils provide. This potential can only be realized by determining
the amount of SOM stored in soils now, with subsequent quantification of how this is affected by management strate-
gies intended to increase SOM concentrations, and used in soil C models for the prediction of the roles of soils in
future climate change. An apparently obvious method to increase C stocks in soils is to augment the soil C pools with
the longest mean residence times (MRT). Computer simulation models of soil C dynamics, e.g. RothC and Century,
partition these refractory constituents into slow and passive pools with MRTs of centuries to millennia. This partition-
ing is assumed to reflect: (i) the average biomolecular properties of SOM in the pools with reference to their source in
plant litter, (ii) the accessibility of the SOM to decomposer organisms or catalytic enzymes, or (iii) constraints
imposed on decomposition by environmental conditions, including soil moisture and temperature. However, con-
temporary analytical approaches suggest that the chemical composition of these pools is not necessarily predictable
because, despite considerable progress with understanding decomposition processes and the role of decomposer
organisms, along with refinements in simulation models, little progress has been made in reconciling biochemical
properties with the kinetically defined pools. In this review, we will explore how advances in quantitative analytical
techniques have redefined the new understanding of SOM dynamics and how this is affecting the development and
application of new modelling approaches to soil C.
Keywords: C isotopes, decomposition, recalcitrance, soil C models, soil microorganisms, soil organic matter
Received 1 February 2012; revised version received 1 February 2012 and accepted 3 February 2012
uted between soil organic C (1550 Pg C) and soil inor-
Introduction
ganic C (i.e. carbonates, 950 Pg C). The total terrestrial
By the end of the current century, global mean temper- biota contains about 560 Pg C and is the major source
ature is predicted to increase by 2–7 °C, and the of C inputs to the soil organic matter (SOM) pool (Lal,
amount and distribution of precipitation is predicted to 2008; Fig. 1). Organic carbon is the largest single com-
change, due to increases in atmospheric greenhouse ponent of SOM which encompasses not only the contin-
gas concentrations, especially carbon dioxide (CO2; Wu uum from fresh to progressively decaying plant,
et al., 2011). Soils represent a massive stock of poten- microbial and soil faunal debris and exudates but also
tially volatile carbon (C) and act as both a buffer against contains the other elements vital for life, i.e. nitrogen
atmospheric CO2 increase and as a potential sink for (N), phosphorus (P) and sulphur (S). Hereafter, the
additional C depending on the balance between photo- term SOM will be used to cover all references to SOM
synthesis, the respiration of decomposer organisms and and soil organic C. Terrestrial ecosystems offer signifi-
the stabilization of C in soils. The total global stock of C cant potential to capture and hold substantially
in soil is estimated at approximately 2500 Pg C distrib- increased volumes of C within SOM (Smith & Fang,
2010), mainly through the recovery of soil C lost due to
Correspondence: Dr Jennifer A. J. Dungait, tel. + 44 0 1837 883 500; land-use change (Smith, 2008; Powlson et al., 2011) and
fax + 44 0 1837 82 139, e-mail: jennifer.dungait@rothamsted.ac.uk by enhancing the ‘missing C sink’ proposed to exist in
2
Rothamsted Honorary Fellow soils (Canadell et al., 2007). There are indications that
© 2012 Blackwell Publishing Ltd 17811782 J . A . J . D U N G A I T et al.
Huber et al., 2008), although there is little quantitative
Topsoil
evidence for such a threshold (Loveland & Webb,
Biota
2003), and Janzen (2006) proposed that it is the bioavail-
SOC ability of SOM that is the major influence on soil prop-
Subsoil erties. Importantly, the general responses of C stocks in
SIC
terrestrial ecosystems to changes in environmental con-
ditions, especially temperature and precipitation, and
their combined effects, remain unclear (Wu et al., 2011).
Fig. 1 The global distribution of C between soil biota (flora and Three sets of interacting factors, substrate quality,
fauna; 560 Pg), soil inorganic C (SIC; 950 Pg) and soil organic C organisms (including implicitly their combined enzy-
(SOC; 1550 Pg) in the terrestrial C pool (Lal, 2008), showing matic repertoire) and environment (which includes a
division of soil organic C between top-soils (i.e. A horizon relatively poorly understood and frequently over-
~25%) and subsoils (i.e. below A horizon ~75%; Jobbágy & Jack- looked set of abiotic decomposition processes), are the
son, 2000).
main controlling decomposition of organic materials
(Swift et al., 1979). Substrate quality is an abstract term
plants and soils combined annually absorb 1 Pg C more used to describe the ability of SOM: (i) to supply
than they emit, but the reasons are unclear (Janzen, organic molecules for both catabolic (energy conver-
2004). It has been postulated that increasing SOM sion) and anabolic (biosynthetic) metabolism, (ii) to
concentrations in soils up to 2 m depth by 5–15% could supply other nutrient elements to decomposer organ-
decrease atmospheric CO2 concentrations by 16–30% isms, and (iii) the extent to which properties of the sub-
(Baldock, 2007; Kell, 2011). These ideas have led to sub- strate retard its exploitation. These retarding factors
stantial attention being paid to quantifying the stocks of include, for example, being hydrophobic or physically
C in soils, and the mechanisms of stabilizing C in soils, impenetrable, or containing compounds that inhibit
including by land management options, to increase enzyme activity, such as tannins or polyphenol con-
SOM stocks (Lal, 2002; Smith, 2008). Despite the funda- tents that complex with and inhibit enzymes (Freeman
mental importance of reliable estimates of C stocks in et al., 2004; Sinsabaugh, 2010). The ability to assess sub-
soils, estimating them at the global or even a regional strate quality is not easy and the bulk of this review
scale, and more importantly detecting changes in these addresses the biochemical dimensions of this question
stocks, is remarkably difficult for the following reasons: and its importance relative to physical accessibility of
(i) mismatches between the temporal and spatial reso- the SOM to decomposer organisms or extracellular
lution of the survey and analytical data, (ii) the natural (exo-) enzymes as a constraint on decomposition.
temporal and spatial variability in soils, (iii) the relative The response of different ecosystems to changes in
paucity of data on the variations in soil depth and dis- temperature has attracted much attention and obtain-
tribution of C with depth, and (iv) the fact that key ing definitive evidence of its effects on SOM decompo-
parameters, such as soil depth (particularly for the sub- sition has proved remarkably difficult to obtain, yet the
soils) and bulk density have often not been recorded, response of decomposition to temperature change is
which compromises the conversion of concentration intimately linked to the recalcitrance of SOM. It is
data into amounts of SOM (Hopkins et al., 2009). bizarre but true that, depending on the experimental
Added to these compounded operational difficulties is approach used and the particular aspect of decomposi-
the fact that accurate assessments of SOM change are tion being investigated, it is possible to find reports
bedevilled by all the problems of determining a very demonstrating that increases in temperature have a
small difference between two very large values. strong positive effect (Fang et al., 1998; Knorr et al.,
Soil organic matter is critical to ensure secure food 1998) or no effect on decomposition (Liski et al., 1999;
production; the process of decomposition is key to the Giardina & Ryan, 2000), or even a negative effect on
recycling of macronutrients, i.e. N, P and S, into plant- long-term decomposition (Dalias et al., 2001). The main
available forms, and its effective management can reason given for these paradoxical observations is that
reduce the need for fossil fuel consumption to supply SOM is not a single pool of biochemically or kinetically
N fertilizer. A wide range of soil properties, including uniform molecules (Knorr et al. 1998). Traditional
soil structure, water and nutrient holding capacity and kinetic theory predicts that while more ‘chemically
biodiversity, are improved by maintaining optimal recalcitrant’ compounds will decompose more slowly,
quantities of SOM (Watts et al., 2006; Powlson et al., their decomposition should also be more temperature
2011). A SOM concentration of less than 2% is consid- sensitive (Ågren & Bosatta, 2002). Although apparently
ered to be the threshold value below which soil func- a simple concept governed by the van’tHoff principle,
tion is impaired (Greenland et al., 1975; Lal, 2004; the effects of changes in temperature on the decomposition
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 1781–1796S O I L O R G A N I C M A T T E R T U R N O V E R 1783
of SOM and nutrient mineralization in soils have pro- also respond to altered environmental conditions which
ven remarkably difficult to quantify (Kirschbaum, may change C inputs to soil (Dungait et al., 2010). The
2006). Although it is well established that, within quantity and quality of SOM entering soils may be sub-
reasonable limits, the biological processes which drive stantially altered depending on how the combination of
decomposition will be more rapid at greater tempera- changes in temperature and moisture regime affect pri-
tures, being able to assign a thermal coefficient or set of mary production, and the regulatory cascades that
coefficients to decomposition and nutrient mineraliza- affect other ecosystem processes, such as nutrient avail-
tion has proved remarkably difficult (Davidson & Jans- ability and herbivore abundance, which regulate
sens, 2006). It is a widely held concept that ‘recalcitrant’ production indirectly (Wookey et al., 2009).
SOM is more sensitive to changes in temperature than
‘labile’ SOM (Bauer et al., 2008) on the grounds that a
Can pools in soil C models be defined according to
higher resistance to decomposition (Ea, activation
molecular structure?
energy) is associated with the energetics of decomposi-
tion. The warmer the environment, the more likely the The most widely applied SOM simulation models, e.g.
critical value of Ea is to be exceeded. Such effects are Century and RothC, divide SOM into pools (Table 1)
taken up in models but it is difficult to infer both differ- with varying intrinsic decomposition rates that are
ences in rate of decomposition and rate of change with rationalized by assuming that a combination of bio-
temperature for multiple pools or qualities of SOM chemical and physical properties control decay (Adair
from data which are necessarily sparse because it is et al., 2008; Kleber, 2010). However, the relative contri-
long term. Experiments which removed ‘labile’ SOM butions of the biochemical and physical controls on
(Conant et al., 2008a,b) support increased temperature decay are rarely tested empirically and the pools are
sensitivity of the remainder. However, there are three usually only defined kinetically. Assumed mean resi-
more significant remaining challenges in understand- dence times (MRTs) of different SOM pools are used to
ing and modelling the effects of climate change on partition the highly complex, dynamic process of SOM
SOM turnover. First, there is the practical difficulty of turnover into a series of soil C fluxes from the pools.
disentangling the effects on the decomposer communi- This partitioning is supposed to reflect the average bio-
ties of relative depletion of the most accessible compo- molecular and physical properties of SOM in the pools
nents of the SOM, from the direct effects of temperature (e.g. metabolic, structural and recalcitrant) or the
on the metabolism of soil microorganisms (Hartley accessibility of the SOM to decomposer organisms or
et al., 2007). Second, there are conflicting reports about catalytic enzymes, or constraints imposed on decompo-
whether soil microorganisms adapt to increased tem- sition by environmental conditions. However, percep-
peratures by down-regulating respiration (Bradford tions of the stability of particular plant compounds
et al., 2008; Hartley et al., 2008, 2009). Third, plants will often appear to reflect the roles that the different molec-
Table 1 The pools of SOM defined according to their mean residence times (MRTs; Jenkinson & Rayner, 1977; Paustian et al.,
1992) and corresponding compound classes (Brady & Weil, 2002)
Residue type Century RothC Residence time (years) C:N Compounds
Litter Metabolic DPM 0.1–0.5 10–25 Simple sugars
Amino acids
Starch
Structural 2–4 100–200 Polysaccharides
SOM Active BIO 1–2 15–30 Living biomass
DPM POM
Polysaccharides
Slow RPM 15–100 10–25 Lignified tissues
Waxes
Polyphenols
Passive HUM 500–5000 7–10 Humic substances
IOM Clay: OM complexes
Biochar
DPM, decomposable plant material; BIO, microbial biomass; RPM, resistant plant material; HUM, humified organic matter; IOM,
inert organic matter; POM, particulate organic matter; OM, organic matter.
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 1781–17961784 J . A . J . D U N G A I T et al.
ular structures perform within the plant, and how vided through analytical advances in tracking the fate
humans manipulate them for their benefit, i.e. glucose of specific organic compounds which are associated
in energy drinks, lignin in wooden structures and with pools in soil C models, reported as the outcomes
waxes as preservatives. Thus, strategies for increasing of experiments that have explored the fate of meta-
C stocks in soil suggest the enhancement of inputs of bolic, structural and recalcitrant compounds from
biochemically recalcitrant ‘biomacromolecules’ as a plant litter in soils (Amelung et al., 2008).
management tool to augment stable SOM stocks (Lor-
enz et al., 2007), although an overall dilemma associ-
Metabolic compounds
ated with soil management for C sequestration is
presented by Janzen (2006): ‘Shall we hoard [soil C] or Metabolic compounds are usually low molecular
use it?’, since SOM is also the source of fertility. How- weight, highly labile compounds, such as simple sug-
ever, the stability of plant compounds outside the soil ars, organic acids including amino acids, which may
does not necessarily imply stability within the soil. derive directly from plants, e.g. photosynthate and rhi-
Microorganisms are in a constant state of ‘starvation’ in zoexudates, proteins and storage carbohydrates, e.g.
the soil environment where substrate supply is spo- starch and fructans (Hopkins & Dungait, 2010). They
radic both in time and space (Dungait et al., 2011), and may also derive secondarily from microbes as a result
highly adapted, complex decomposer communities of exudation and excretion, cell death and decay (Hof-
have evolved in soils to tackle any SOM that is encoun- man & Dusek, 2003). Metabolic compounds that are
tered. been applied to soils in vitro can decompose very
Empirical evidence is building against the notion of quickly, presumably because they are rich in energy,
intrinsic molecular recalcitrance as a concept in under- readily accessible to organisms and rapidly assimilated;
standing the stability of SOM (see recent reviews by the half-life of amino acids and simple sugars can be
Kögel Knabner et al., 2008; Marschner et al., 2008; less than 1 h in surface soil horizons (Boddy et al., 2007;
Kleber, 2010; Schmidt et al., 2011) although this Hill et al., 2008). These compounds are therefore associ-
attitude is not new (Jenkinson & Rayner, 1977; Sollins ated with the ‘active’ and ‘metabolic’ pools in the Cen-
et al., 1996), with opinion turning away from the tury model, and the DPM (decomposing plant
idea that the very old SOM in soils is inherently resis- material) and BIO (biomass) pools in the RothC model
tant to biological attack (Jenkinson et al., 2008). Recent (Table 1). Paradoxically, although easily biodegradable
biogeochemical analyses of organic compounds metabolic compounds actually constitute a substantial
assigned to the pools in soil C models have revealed component of SOM (Derrien et al., 2007), the BIO and
that SOM does not comprise pools of biochemically or DPM compartments are small in RothC model. Recent
kinetically uniform molecules (Davidson & Janssens, evidence also shows that apparently easily biodegrad-
2006; Kirschbaum, 2006). Evidence from the diversity able metabolic compounds may be older than bulk
of compound-specific responses to experimental SOM (Gleixner et al., 2002; Derrien et al., 2006) and
manipulation in different soils suggests that recalci- become stabilized for millennia in the ‘passive’ SOM
trance cannot be intrinsic to specific compounds (Ame- pool (Paustian et al., 1992).
lung et al., 2008). For example, SOM in fast cycling
fractions comprises a mixture of plant compounds
Structural compounds
including plant lignins (‘recalcitrant’ compounds;
Table 1) as well as carbohydrates (‘metabolic’ or ‘struc- Polysaccharides are described as ‘structural’ com-
tural’ compounds; Table 1; Derrien & Amelung, 2011). pounds in plant litter presumed to enter the ‘active’
Thus, Kleber (2010) argued that ‘recalcitrance’ is a pools in the Century model, and DPM in RothC (Brady
semantic term without a mechanistic foundation, even & Weil, 2002). Cellulose and hemicellulose polysaccha-
though it has empirically derived meaning. Von Lüt- rides are the most abundant substrates in plant litter
zow & Kögel-Knabner (2010) contended that the value (Dungait et al., 2005; Jia et al., 2008), and amino-
of the concept of recalcitrance is the ability to differen- polysaccharides, including N-acetylglucosamine and
tiate between the decomposability of organic mole- muramic acid, are abundant in the peptidoglycan of the
cules, although Von Lützow et al. (2006) concluded bacterial cell envelope and the chitin of fungal cell
earlier that recalcitrance appears to be a property of walls. It is perhaps surprising that there is little empiri-
SOM that allows it to resist decomposition for years cal evidence for their specific decomposition dynamics,
rather than centuries. Overall, the diverse mechanisms although it is their very ubiquity and relatively simple
for explaining this difference begs for a more quantita- chemistry which confers challenges in determining
tive understanding of the relative importance of the their turnover dynamics in soils. Strong acid hydrolysis
mechanisms involved (Kleber, 2010). This is being pro- is widely used to extract total sugars from soils making
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 1781–1796S O I L O R G A N I C M A T T E R T U R N O V E R 1785 it difficult to distinguish between the monomers of Schmidt, 2007). Indeed a recent review concluded that ‘structural’ polymers of plant or microbial origin, and the literature is contradictory with regard to lignin alternative sources including ‘metabolic’ compounds decomposition rates but supported the idea that most (see Metabolic compounds above), even if the plant or decomposed within 5 years (Thevenot et al., 2010). Bas- polysaccharide is 13C or 14C (radiocarbon) labelled idiomycetes are the major biotic decomposers of lignin, (Cheshire & Mundie, 1990; Derrien et al., 2006; Dungait of which only the white rot fungi are capable of its com- et al., 2009). Many bacteria and fungi degrade plant plete mineralization to CO2 and H2O, and then only in polysaccharides through the hydrolysis of the glyco- aerobic environments (Robertson et al., 2008). However, sidic links using exo-enzymes, e.g. cellulase and other soil organisms are important in partial lignin xylanase. It has been determined that 60% of cellulose breakdown and modification, and may operate even is mineralized in soil after 1 month, with an additional under anaerobic conditions (Chen et al., 1985). Actino- 7% decomposed within 3 months (Derrien et al., 2007), bacteria are considered to be responsible for up to 15% and the remainder persisting in soils long-term (Gleix- of lignin degradation in soil; although they cannot com- ner et al., 2002; Quenea et al., 2005). Because of the wide pletely mineralize lignin they solubilize the polymer to range of generalist and specialist soil microorganisms gain access to the associated polysaccharides (Dignac that use polysaccharides as a substrate (Fontaine & et al., 2005). Xylanases disrupt hemicellulose-lignin Barot, 2005), it is unlikely that ‘structural’ compounds associations, without mineralization of the lignin per se, persist intact in surface soil horizons unless they subsequently making the lignin more readily available become protected from decomposition. Cheshire (1977) to direct digestion, and Vane et al. (2001) proposed that pointed out more than 30 years ago that it is the hemicellulose degradation is required for efficient lig- inaccessibility to enzymes, not recalcitrance, which is nin degradation. New insights into the structure of the responsible for the slow degradation of polysaccharides lignin macromolecule also suggest that lignin biosyn- in soil. For example, it has been suggested that soil thesis is not random (Reale et al., 2004). Well-defined polysaccharides play a key role in the stabilization of chain configurations identified in lignin macromole- soil microaggregates (
1786 J . A . J . D U N G A I T et al.
no doubt that a proportion of n-alkanes are stabilized tively (Table 1). Biomass-derived black C comprises a
in soil long-term: Bol et al. (1996) determined that the substantial component (5–50%) of organic C in some
aliphatic hydrocarbon fraction from a peaty soil was soils, and is assumed to decompose at a much slower
around 14 000 years old, confirming the potential for rate than SOM due to its highly condensed aromatic
n-alkanes to be sequestered for millennia in soils structure (Schmidt et al., 2001). Large charcoal particles
under particular conditions. This has been indepen- originating from forest wildfires can remain in soils for
dently confirmed by a wide range of solid-state 13C- thousands of years (Major et al., 2010), although smaller
nuclear magnetic resonance (NMR) studies (Baldock particles derived from grassland burning can hardly be
et al., 1991). detected in steppe and prairie soils (Forbes et al., 2006).
Lehmann et al. (2006) suggested that conversion of bio-
Humic substances. Humic substances are obtained from mass C to biochar leads to sequestration of about 50%
soil as humic acids and fulvic acids by simple extrac- of the initial C yielding more stable soil C than burning
tion with strong alkalis and acids, with the residue or direct land application of biomass. However, biochar
‘humin’ as the non-hydrolysable fraction assumed to can be used as a substrate by soil microorganisms
equate to the most refractory SOM. However, these are (Wengel et al., 2006) and is therefore not completely
operationally defined chemical fractions with no real inert. However, it is difficult to evaluate the factors con-
relevance in ecological terms (Wander, 2004), and it is trolling its breakdown because there are significant
well documented that such preparations contain variations in the physicochemical structure and compo-
artefacts from sample preparation and are entirely non- sition of biochar that arise due to differences in starting
selective with respect to biological entities in soils material and pyrolysis conditions (Li et al., 2006; Krull
(Baldock et al., 1991). For a long time the formation of et al., 2009; Asadullah et al., 2010; Smith et al., 2010b).
recalcitrant humic substances created through sponta- After application to soils, biochar decomposition rates
neous reactions between small reactive metabolites, or vary under different soil conditions, e.g. water regime
oxidative cross-linking with biomacromolecules result- (Nguyen & Lehmann, 2009), native SOM concentrations
ing in new condensation products or restructured com- (Kimetu & Lehmann, 2010) and pH (Luo et al., 2011).
pounds, has been considered as the major pathway for Clearly, any increase in C sequestration due to biochar
SOM stabilization (Piccolo, 2001). Heterogeneity in size incorporation would be further diminished if there
and chemistry is assumed to make such amorphous were a positive priming effect on SOM caused by bio-
polymers resistant to enzyme attack (Marschner et al., char addition, or if there were an increased mineraliza-
2008). Thus, humic substances are assigned to the ‘pas- tion of biochar following the introduction of a substrate
sive’ (Century) and ‘HUM’ (RothC) pools, with MRTs (Luo et al., 2011). Indeed, stimulation of biochar miner-
of 500–5000 years (Table 1). Stevenson (1982) recog- alization in soil by the addition of glucose to a biochar
nized much earlier that humic substances are readily amended soil has been reported (Hamer et al., 2004;
degradable when extracted from soils, which leads one Kuzyakov et al., 2009), although no effect was observed
to assume that another mechanism must be responsible following the addition of cellulose (Nocentini et al.,
for the stability of their molecular constituents within 2010). Losses of native SOM have also been determined
the soil. Thus, the view that novel macromolecules arise after addition of biochar (Wardle et al., 2008; Zimmer-
from random condensation reactions in soils has given man et al., 2011). Overall, the use of biochar as a robust
way to the point of view that ‘humic substances’ are in strategy to increase soil C stocks as described by Love-
fact mixtures of partially decomposed plant and micro- lock (2009) requires additional investigation.
bial biomass that are inaccessible to soil microorgan-
isms (Kelleher et al., 2006; Von Lützow et al., 2008).
The role of soil organisms in SOM dynamics
Black C and biochar. ‘Black C’ is the charred remains of Carbon dioxide emissions from autotrophic (root) and
plant material which appears in soils as a result of heterotrophic (microorganisms and fauna) soil respira-
human activity and natural fires. Biochar is a similar tion are an order of magnitude greater than those from
material produced by oxygen-limited pyrolysis of bio- human activities, such as fossil fuel burning (Nielsen
mass, organic waste or other feedstock which is pro- et al., 2011). Soil microorganisms, and implicitly their
posed as a soil amendment that is sufficiently combined enzymatic repertoire, demonstrate massive
recalcitrant to aid C storage in soils, as well as confer- physiological and biochemical capacity and are present
ring potential chemical and physical benefits on soil in vast numbers. These factors have led to two pieces of
functions (Krull et al., 2009). Black C and biochar are environmental microbiological dogma: (i) that the soil
assigned to the ‘passive’ and ‘inert organic matter’ microbial community is collectively infallible in terms
(IOM) pools of the Century and RothC models respec- of the range of organic molecules it can degrade, and
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 1781–1796S O I L O R G A N I C M A T T E R T U R N O V E R 1787
(ii) the capacity to degrade any substrate exists in has been relatively little attempt to integrate models of
almost any soil. These ideas owe much to the early food webs with more general models of C turnover (De
work of Baas-Becking and Beijerink: ‘everything is Ruiter et al., 1994; Fitter et al., 2005). Brussaard et al.
everywhere, but the environment selects’ (de & Bouvier, (2007) suggest a conceptual framework for doing this,
2006), coupled with the diverse range of enzymes of acknowledging that the issue of the different scales of
both bacteria and fungi. Although probably not strictly macrofaunal and microbial action must be taken into
accurate, they are good enough working assumptions account, and Blanchart et al. (2009) describe how an
because microorganisms or microbial consortia capable ‘agent-based’ modelling approach can simulate the
of degrading any natural compound and many xenobi- effects of earthworms on soil structure. A similar
otic compounds can be enriched from soil communities. approach might be able to reconcile the many different
The diversity of microorganisms in a soil at Rothamsted scales at which soil biota act on SOM.
starved of inputs for 50 years appears no different from
an adjacent SOM-rich pasture (Hirsch et al., 2009). The
If all SOM is decomposable, what preserves it?
large diversity and abundance of soil microorganisms
is undoubtedly a result of a long evolutionary history Some degree of chemical recalcitrance as a stabilization
and the vast number of spatial and environmentally factor of SOM in soils cannot be ruled out (Von Lützow
distinct niches in soils. Moderating factors such as plant & Kögel-Knabner, 2010). The concentrations of aro-
diversity will interact with microbial diversity through matic and double-bond hydrocarbons increase with
factors such as the timing, composition and abundance depth whereas other compounds, such as single-bond
of residue and exudate supply (Scherber et al., 2010), alkyl C hydrocarbons, tend to decrease (Eusterhues
and the opportunities for symbioses, such as mycorrhi- et al., 2007; Spielvogel et al., 2008). Ellerbrock & Gerke
zas. Most models assume that changes in the microbial (2004) found that coatings of C on aggregates in the
community have limited effects on soil processes (Con- subsoil contained hydrophobic substances which con-
dron et al., 2010), and consequently the role of the soil tributed to aggregate stability. However, overall it
microbial community that is acknowledged overtly in appears that if soil microorganisms can access SOM,
the BIO pool of the RothC is a pool with short MRT they are able to degrade it relatively rapidly, i.e. within
(Table 1). However, C from SOM incorporation into years or decades. The major C stabilization mechanisms
soil microorganisms can be C being repeatedly recycled in soils are now recognized to be ‘biologically non-pre-
through, and conserved within, the microbial biomass ferred soil spaces’ (Ekschmitt et al., 2008) where SOM is
(Rinnan & Bååth, 2009). physically protected from microbial activity regardless
The activity of soil microorganisms, and therefore the of its initial chemical structure (Kleber et al., 2011). Van
potential to decompose SOM, is often facilitated by soil Veen & Kuikman (1990) and Von Lützow et al. (2006)
meso- and macroinvertebrates (nematodes, enchytrae- listed the mechanisms involved in physical preserva-
ids, collembola and lumbricids). This is done by physi- tion of SOM as (i) occlusion within aggregates, and (ii)
cal conditioning of the substrate by comminution adsorption onto minerals, but also a third mechanism
(which increases the surface to volume ratio), wetting has been postulated: (i) substrate-driven ‘biological rate
and the application of surfactants, mixing with soil limitation’ (e.g. Ekschmitt et al., 2005).
components leading to incorporation (thereby remov-
ing SOM from the extremes of temperature and desic-
Physical protection – aggregates and organomineral
cation at the surface), and by inoculation with soil
complexes
microorganisms (Wolters, 2000). Conversely, they can
also process labile compounds into more stable entities The mechanisms involved in physical preservation of
(Fox et al., 2006; Rawlins et al., 2006, 2007). Earthworms SOM are occlusion within aggregates and adsorption
are particularly important agents of SOM decomposi- onto minerals (Six et al., 2000). The literature associated
tion in most terrestrial ecosystems, accelerating rates of with these mechanisms is particularly rich, and we
comminution and dispersal through feeding activities, offer a summary herein, and refer the reader to the
although whether their activity is a net sink or source many excellent references cited in this section.
of C is under debate (Oyedele et al., 2006; Don et al., Adsorption onto minerals is a much more intimate
2008; Ekschmitt et al., 2008; Hong et al., 2011). 13C stable association between SOM and other soil components
isotope analyses of soil invertebrates have revealed that than the occlusion mechanisms. Sorption between SOM
different species exhibit dietary preference and trophic and clay minerals and both amorphous iron and amor-
niche exploitation of the same SOM resource (Dungait phous aluminium colloids plays a major role in preser-
et al., 2008b; Murray et al., 2009; Pollierer et al., 2009; vation due to their large, charged surface areas
Crotty et al., 2011). Despite these observations, there (Kiem & Kögel Knabner, 2002; Six et al., 2002). Such
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 1781–17961788 J . A . J . D U N G A I T et al. organomineral associations render SOM protection gate formation (Krull et al., 2004). Aoyama et al. (2000) because the adsorption affinity to the mineral exceeds added 13C-labelled glucose to soil and found that the that of the enzyme active site. Organomineral com- majority of the 13C was assimilated by soil microorgan- plexes are likely to be the primary mechanism whereby isms in soil macroaggregates after 14 days. Polysaccha- SOM is stored for millennia, and their assignment to rides exuded from fungal hyphae, bacteria and roots the ‘passive’ pool in the Century model (Table 1) adsorb strongly to negatively charged soil particles appears to be well deserved. Large amounts of C with through cation bridging, binding together individual old radiocarbon ages are found in association with size soil particles and microaggregates into macroaggre- fractions
S O I L O R G A N I C M A T T E R T U R N O V E R 1789
scarce energy reserves to remain ‘metabolically alert’, SOIL
this strategy enables some microorganisms to respond Microbe or
rapidly to fresh substrate when it becomes available, exo-enzyme
conferring a competitive advantage over microorgan-
isms the survival strategy of which is based upon true
dormancy (Dungait et al., 2011). The need for a slow
trickle of organic molecules from SOM to maintain the
survival of soil microorganisms has subsequently led to
the suggestion that there is an abiotic bottleneck (the
‘Regulatory Gate’) that regulates a sustained, but lim- Organic
ited supply of SOM to soil microorganisms (Kemmitt Dessicated matter Waterlogged
et al., 2008). H2O/O2 availability
Soil structure and aggregation may control the sup-
Fig. 2 The ‘random walk’ theory representing the controls of
ply of water, nutrients and oxygen, and the connectiv- decomposition of soil organic matter (SOM) as a function of
ity between C and potential decomposers (Eusterhues accessibility by microorganisms in the soil matrix. The probabil-
et al., 2007; Kuka et al., 2007; Bachmann et al., 2008). ity of access of microbe to organic matter in the soil matrix is
Sinsabaugh & Follstad Shah (2011) proposed a concep- controlled by a combination of biological, physical and chemical
tual model in which the recalcitrance of SOM is a variables. The pathway (indicated by dotted lines) connecting
function of its relative susceptibility to a succession of the decomposer microorgansim or exo-enzyme with the organic
exo-enzymes, the activity of which is limited by the matter is the ‘route’ that has to be ‘navigated’ multi-dimension-
movement of substrate, enzyme and organism. Kuka ally before the organic matter decomposes. Examples of the
et al. (2007) modelled SOM decomposition in terms of dimensions that have to be navigated include the metabolic
energy level of the microorganism, the motility of the microor-
the pore-space in soil, arguing that decomposition can
ganism or the movement by the exo-enzyme, the spatial separa-
only be achieved when water, oxygen, substrate and
tion of the microorganism or the exo-enzyme and the organic
organism/enzyme come together, and the organisms matter, pH, temperature, soil pore size, length, connectivity and
can only benefit if there is a transport connection to tortuosity, strength of SOM sorption to soil particles, occlusion
enable metabolites to travel back to the same organism between clay layers and within aggregates, efficiency of enzyme
from the site of enzyme action. These ideas marry well activity, stearic hindrance, and the requirement for synergy
with the Regulatory Gate Hypothesis (Kemmitt et al., with other enzymes. The shading around the substrate indicates
2008) where decomposition is thought to be limited by the abiotic release of components of organic matter (after
factors other than the activity of microorganisms. One Kemmitt et al., 2008).
key substrate-enzyme interaction has attracted much
attention. Tannins and polyphenols complex with pro- ple, freeze-thaw and wet-dry cycles, or bioturbation,
teins and inhibit the activity of soil enzymes, except the potential for decomposition is likely to depend on
polyphenol oxidase, which is limited by low pH and the mean length of a ‘random walk’ by the decomposer
low oxygen status (Freeman et al., 2001, 2004). Based on organisms through tortuous soil pore space (Fig. 2).
the behaviour of polyphenolic compounds and the Physical variables include the distance between micro-
enzymes that catalyze their oxidation, Sinsabaugh organisms and substrate; soil pore size, length, connec-
(2010) proposed that cool, wet, anaerobic soils should tivity and tortuosity (Kuka et al., 2007); and, physical
accumulate C and that warm, dry, aerobic soils should protection of the substrate, i.e. strength of sorption to
lose it. Although observations generally bear out this soil particles and occlusion between clay layers and
proposal the key intervention would be to remove phe- within aggregates. Once within the vicinity of substrate,
nols from peat or preserve them in arid soils. exo-enzymes might accelerate decomposition, but this
If all soil SOM is degradable in principle, the con- will be metabolically uneconomic if the pathway of the
straints on microbial decomposition of SOM in soil digested substrate back to the microorganism is equally
probably depend on the co-occurrence of water, air, long and tortuous. The efficiency of enzyme activity
substrate and microbe at the same point in space and will be compromised by stearic hindrance, the require-
time. Van Haastert & Bosgraaf (2009) described the ment for synergy with other enzymes, pH and tempera-
food-searching strategy of starving organisms in heter- ture. If the Regulatory Gate hypothesis of Kemmitt
ogeneous environments, as progressively longer ‘ran- et al. (2008) is correct, a small but sustained abiotic
dom walks’, probably because there is no information release of SOM (indicated by the shadow around the
about substrate availability (Hénaut et al., 2002; substrate source in Fig. 2) may also to contribute to the
Edwards et al., 2007; Reynolds et al., 2011). Thus, in the likelihood of an encounter between soil microorganisms
absence of physical disturbances caused by, for exam- and SOM.
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 1781–17961790 J . A . J . D U N G A I T et al.
have found wide use for predictive purposes have
C sequestration in subsoils
tended to be simple and robust (RothC, Coleman et al.,
If accessibility by microbes and exo-enzymes is the key 1997; Q model, Ågren & Bosatta, 1987) or versatile
factor in controlling C turnover in soils, then deeper (Century, Parton et al., 1987). It is widely accepted that
soil horizons may provide an opportunity to enhance C models can only be expected to operate effectively
sequestration. Up to 75% of the C in the soil resides when applied to soil systems for which they were
below the surface horizon (Fig. 1; Jobbágy & Jackson, designed and when applied within the parameter
2000). The deeper SOM is assumed to be very stable, ranges for which they have been validated (Manzoni &
with radiocarbon ages of more than 4000 years Porporato, 2009). This leads to obvious difficulties
reported (Jenkinson et al., 2008), and ascribed in part to when the models are pushed to the edge of, or beyond,
more mineral association and protection at greater their validation, such as may occur when they are
depths (Spielvogel et al., 2008; Chabbi et al., 2009). applied to rapid environmental change or ‘unusual’
Deep soils are more likely to be colder, waterlogged, soils. For example, reductive models, based on long-
anoxic and nutrient-limited compared with surface term agricultural experimental data from mineral-dom-
horizons, leading to smaller and less active microbial inated, low SOM content soils, have their downfalls
communities. The restricted connectivity between and critiques when applied to peats. Although soils
microorganisms and the substrate mentioned above with restricted drainage such as peats contain about
(see Regulation of microbial activity by substrate supply) one-third of the world’s store of soil C, the RothC and
will be more severe in the subsoil (Ekschmitt et al., Century models handle mineral soils only (Chimner
2008; Salomé et al., 2010). However, environmental et al., 2002; Falloon et al., 2006), yet the models are
conditions in subsoils are typically more stable because widely used in global studies of soil C dynamics.
they are buffered from rapid changes in moisture and ECOSSE (Smith et al., 2010a), based on RothC, and
temperature, and therefore provide a nutritionally MILLENNIA (Heinemeyer et al., 2010), which uses a
and energetically impoverished but stable set of niches cohort approach similar to that in the Q model (see
for microorganisms, compared with surface soils below) are recent attempts to rectify this failing.
(Sanaullah et al., 2011). Models of C turnover are the only reasonable
Kell (2011) recently suggested the potential to approach available for the prediction of the roles of
enhance C storage through the development of deep- soils in future climate change. To date, Global Ecosys-
rooted plants that would incorporate C directly into the tem Models vary in the way they treat differences in
subsoil. Rasse et al. (2005) described the preferential the decomposition of soil C. As an illustration of some
stabilization of root C compared to shoot C in soils. of the difficulties, Jenkinson & Coleman (2008) sug-
However, the principal obstacles to C incorporation to gested that emission of CO2 from soils as a result of glo-
subsoils by deep rooting plants is the mechanical bal warming by modelling subsoil C in the same way
impedance offered by the soil, and the facts subsoils are as surface C may have been over-estimated, and pro-
not usually environmentally favourable for root growth posed a ‘layered’ approach which requires additional
and sometimes offer only limited resources to the development. Friedlingstein et al. (2006) found that
plants. Deep root penetration may also contribute to between one and nine soil organic C pools were used in
priming the decomposition of otherwise stable subsoil different modes, but that all the models considered
C (Fontaine et al., 2007; Marschner et al., 2008; Xiang adopted a pool approach rather than that of quality
et al., 2008; Chabbi et al., 2009; Salomé et al., 2010). continuum. Both the Van Veen & Paul (1981) and
Despite this interest there is remarkably little data that Century models conceive fresh plant material as an inti-
trace the dynamics of carbon in subsoil (Gregory et al., mate mixture of components that differ in decompos-
2011) and the mechanisms that would stabilize carbon ability, such that the decomposition of two easily
or release it require investigation before the potential to decomposable components is restricted by the remain-
store carbon can be exploited. ing skeleton of a third, which is identified with lignin.
Total decomposition is thus retarded in this scheme
because the lignin gradually becomes a greater and
Linking soil biogeochemical understanding with
greater proportion of the remaining substrate and its
soil C modelling
structure impedes the ability of microorganisms to find
To date, the new and emerging ideas on C turnover in the easily decomposable substrates. Whitmore & Matus
soils expressed above have had mixed uptake in quan- (1996) have suggested a simpler function that traces the
titative or predictive computer simulation models, ratio of two components only to achieve the same
although complex models can work well with results effect. Alternatively, the Q model uses a ‘continuous-
from controlled experimental systems. Models that quality theory’ approach that dispenses with artificial
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 1781–1796S O I L O R G A N I C M A T T E R T U R N O V E R 1791
pool classification and attempts to take account of the decomposing low concentrations of starch in soil (Ger-
complete biochemical spectrum of compounds in the man et al., 2011) are examples of kinetic behaviour
SOM from labile to stable, and SOM quality as a mea- other than first-order in soils. In short, if the kinetics
sure of substrate availability to decomposers (Ågren & differs from assumption, SOM can appear more or less
Bosatta, 1987). This may be particularly advantageous decomposable than expected. Given the hard-won and
when modelling soil C under changing climatic condi- rare nature of long-term SOM decomposition data, it
tions, because of the likely alterations in substrate qual- would be surprising if the kinetics of turnover were not
ity, above and below-ground allocation, and ecological subject to considerable uncertainty. Reliable means to
and physiological responses by the both plants and infer mechanisms conclusively from sparse data are
decomposer organisms. lacking and it is probably for this reason that relatively
The RothC model simulates physical protection by simple, robust models of soil processes such as RothC
means of clay, which diverts a greater proportion of C and Century have found wide application in modelling
turn over to the slowly turning over HUM fraction the turnover of C in soils.
rather than CO2. The Van Veen (1981) model models
protection explicitly with factors that increase protec-
Conclusion
tion with clay content. Both models include a very sta-
ble fraction similar to the Century model, but whereas After the geological and marine C pools, the terrestrial
this may itself decompose in the Century and Van Veen pool is the largest global store of C, and has the poten-
models, stable SOM is inert in RothC. These inert or tial to increase thus improving soil quality as well as C
passive pools are necessary to simulate the very old storage. However, the size of the pool changes in time
radiocarbon age of soils (Jenkinson & Rayner, 1977). as a result of environmental change and can only be
Hassink & Whitmore (1997) took the concept of physi- estimated with limited accuracy, especially for subsoils.
cal protection of a portion of the SOM further and mod- The evidence against mechanisms for C stabilization
elled the physical protection in a dynamic way. In their based on initial molecular structures has grown, partic-
model, protected SOM does not decompose but must ularly in the past decade, with advances in analytical
become free before it can do so. Protection and release technologies for tracking the fate of specific labelled
were modelled in analogy to a sorption isotherm with organic compounds in soils. Inconsistencies between
the assumption that soils’ ability to protect C can predicted and measured SOM values have been identi-
become saturated. The success of these models (espe- fied indicating that soil C dynamics are more complex
cially Century and RothC), especially their use in simu- than previously thought and that our models need to be
lating Global Environmental Change and national improved. Specifically, the concept of biochemical recal-
inventories of C stocks and emission of CO2, is support citrance, wherein molecular structures are inherently
for the mechanisms they contain and that physical pro- resistant to microbial decomposition, has been widely
tection in particular better describes the stability of accepted because it has empirical meaning but it is now
organic C in soil than long-term chemical recalcitrance. called into question because of the lack of an adequate
Nevertheless, the need for inert organic C in the RothC molecular and mechanistic definition. If the probability
model points to the existence of small amounts of for SOM decomposition is low in most soils, because of
long-lived C in soil, which is presumed to derive from the requirement for a suite of biological, physical and
black C. chemical conditions to be met, this might explain the
The relative recalcitrance or lack of decomposability paradox that soils contain very large amounts of ancient
of SOM can sometimes be more apparent than real. but apparently decomposable SOM. This new under-
There is often an assumption among modellers that standing suggests that the search for the ‘holy grail’ of
decomposition of SOM is proportional to the amount inherently stable C in soils may be a hopeless quest, and
present, i.e. first-order kinetics. Even Michaelis–Menten our attention should be diverted to the proper manage-
kinetics describing the activity of enzymes approximate ment of SOM, including the rejuvenation of the many
first-order if the substrate is abundant relative to the degraded soils worldwide, particularly those resulting
enzyme. However, Schimel & Weintraub (2003) have from inappropriate land management.
suggested that conditions in soil are such that the enzy- There is a critical need to develop a chain of related
matic capacity concentration may be greater than the hypotheses that express current understanding and
substrate concentration, and Whitmore (1996) has point to critical experiments to calibrate and validate
shown how second or partial order kinetics can explain these ideas. Some questions that could be used to frame
observations better than first-order. Data on the turn- such hypotheses are given below. The list is certainly
over of the soil microbial biomass (Dalenberg & Jager, not definitive, but is intended to highlight some of the
1989) or the reduction in the inducibility of enzymes major areas of uncertainty within known mechanisms,
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 1781–17961792 J . A . J . D U N G A I T et al.
and open questions where new conceptual thinking
Acknowledgements
may be required to link understanding of the biological,
chemical and physical mechanisms with modelling to This work represents part of the BBSRC-funded programmes at
improve predictive capacity particularly in a global Rothamsted Research on Sustainable Soil Function and Bioener-
gy and Climate Change. DWH acknowledges NERC research
change context
grant support (NE/D00893X1 and NE/H022503/1). The authors
1. If decomposition requires the combination of sub- would like to thank the two anonymous reviewers for their
strate, enzymes (microorganisms), oxygen, water and comprehensive reading of the manuscript and constructive sug-
heat, explicit modelling of all these factors in space and gestions for its improvement.
time should improve the predictability of SOM turn-
over.
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